Photoperiodic Clock Research Articles

Photoperiodically Driven Changes in Fos Expression within the Basal Tuberal Hypothalamus and Median Eminence of Japanese Quail

The rapid photoperiodic response in Japanese quail is so precise that it allows neural analyses of how photoperiodic information is transduced into an endocrine response. After transfer from short [SD; 6L:18D (6:18 hr light/dark cycle)] to long (LD; 20L:4D) days, luteinizing hormone (LH) first rises 20 hr after dawn. Using Fos immunocytochemistry, we examined the basal tuberal hypothalamus (BtH) to determine the relationship between brain cell activation and the first endocrine changes. Two separate cell populations within the BtH expressed Fos-like immunoreactivity (FLI) by hour 18 of the first LD. Importantly, this activation occurred before the LH rise. Median eminence activation appeared within glial cells, whereas activated infundibular nucleus cells were neuronal, providing support to the view that gonadotropin-releasing hormone (GnRH) release can be controlled at the terminals by glia. The FLI induction parallels LH changes, suggesting that gene expression may be involved in events preceding photostimulation and is the earliest photoperiodically stimulated physiological change yet reported. Additional experiments provided further support for this hypothesis. First, photoperiodically induced activation is not a result peculiar to castrates because intact birds displayed similar results. Second, the critical length of 14 hr of light had to be exceeded to cause both BtH activation and a LH rise 30 hr from dawn. Finally, valuable evidence of the response specificity was provided by using a unique property of the quail photoperiodic clock in which exposure to 10L:26D, but not 10L:14D, causes photoinduction. The 36 hr paradigm increased both plasma LH and BtH activation.

Rhythmic components of photoperiodic time measurement in the pitcher-plant mosquito, Wyeomyia smithii.

Photoperiodic time measurement regulating larval diapause in the pitcher-plant mosquito, Wyeomyia smithii, varies in a close relationship with latitude. The critical photoperiod mediating the maintenance and termination of diapause is positively correlated with latitude (r 2 = 0.977) among six populations from southern (30-31° N), intermediate (40° N), and northern (46-49° N) latitudes in North America. The developmental response to unnaturally short and to unnaturally long photoperiods declines with increasing latitude, so that longer critical photoperiods are associated with a downward rather than a lateral shift in the photoperiodic response curve. Exotic light and dark cycles of varying period (T) with a short (10 h) photophase and a scotophase ranging from 14 (T = 24) to 62 (T = 72) h, reveal two geographic patterns: a decline in perturbability of the photoperiodic clock with increasing latitude, and no change with latitude in the 21-h period of rising and falling development with increasing T. These results show (1) that there is a rhythmic component to photoperiodic time measurement in W. smithii, (2) that the period of this rhythm is about 21 h in all populations, and (3) that more northern populations show decreasing responsiveness to photoperiod and increasing stability against perturbation by exotic period lengths (T > 24). Previous studies on W.␣smithii indicate that this single temperate species of a tropical and subtropical genus has evolved from south to north. We therefore conclude that the evolution of increasing critical photoperiod in W. smithii during its adaptive radiation into North America has more likely involved the amplitude and not the period of the underlying circadian pacemaker.

Photoperiodic time measurement and related physiological mechanisms in insects and mites.

For over 60 years, many species of insects and mites have been known to respond in an adaptive way to seasonal changes in daylength. Responses to photoperiod allow them to survive periods of unfavorable environmental conditions. Since the early 1950s, light-sensitive and temperature-compensated circadian clocks have also been known to regulate the timing of many events (behavioral, physiological, biochemical) in all eukaryotic organisms, including insects and mites. Over the past 30 years, considerable effort has been directed at elucidation of the nature of the clock mechanism that underlies photoperiodism. Mathematical models using a number of insect systems have been developed that attempt to causally relate the circadian clock to photoperiodic time measurement. Although some experimental evidence supports these circadian-based models, some insects and mites appear to utilize a non-periodic hourglass timer as the photoperiodic clock. Future work in this field would benefit by following the approach that has proven to be very successful in identifying genes and gene products that regulate circadian rhythmicity in Drosophila melanogaster.

Removal of optic lobes of adult blow flies ( Calliphora vicina) leaves photoperiodic induction of larval diapause intact

Blow flies ( Calliphora vicina) surgically deprived of their optic lobes were found to retain the ability to distinguish between short and long day lengths for the production of diapausing or nondiapausing larval progeny. In this species, therefore, the compound eyes and optic lobes are not essential for photoperiodic reception, and the optic lobes cannot be the site of the photoperiodic clock. The brain emerges as a likely location for both functions.

Involvement of the circadian system in photoperiodic termination of diapause in the spider mite Tetranychus urticae

In the spider mite Tetranychus urticae, both diapause induction and diapause termination are under photoperiodic control. Resonance experiments with three strains from different localities in Europe revealed the involvement of the circadian system in the photoperiodic termination of diapause. In all strains the τ-value of the rhythm involved in diapause termination appeared to be shorter than that of the rhythm involved in diapause induction. This may be caused by a change in period length of a circadian oscillator involved in both induction and termination of diapause, or it may indicate that different circadian oscillators affect diapause induction and diapause termination in the spider mite. In previous experiments it has been demonstrated that the photoperiodic clock controlling diapause termination is most probably the same as the one controlling diapause induction. In eight strains of the spider mite, originating from widely different localities in Europe, the critical nightlengths for diapause induction and diapause termination appeared to be identical. Apparently some change occurs in the circadian system between diapause induction and diapause termination, without a concurrent change in photoperiodic time measurement. This makes it unlikely that the oscillator(s) involved in diapause induction and termination would constitute the photoperiodic clock. The results are interpreted according to the so-called non-clock or resonance hypothesis for the involvement of the circadian system in photoperiodic phenomena. Temperature appeared to affect the resonance rhythm of diapause termination differently in different strains of the spider mite: in two strains the rhythm appeared to be temperature compensated, in two other strains it was not. In two strains of the spider mite, originating from the same latitude, critical nightlength appeared to be the same, whereas the period of the rhythm involved in diapause termination differed from 1–3 h among the strains, depending on temperature. These results do not provide evidence in favour of a circadian-based photoperiodic clock in T. urticae. Another effect of temperature was found on the appearance of the different resonance peaks: temperature had little effect on the time course of appearance of the first peak (at nights shorter than the critical nightlength), but subsequent peaks (at nights longer than the critical nightlength) developed faster at higher temperature. This suggests that the mechanism of diapause termination in regimes with nights shorter than the critical nightlength is different from that with nights longer than the critical nightlength. The first represents the photoperiodic response proper, controlled by the photoperiodic clock at nightlengths around the critical nightlength, whereas the latter is most probably a ‘resonance’ effect, revealing the influence of the circadian system on the expression of the photoperiodic response in extended nights. The above effect of temperature therefore also appears to corroborate the non-clock hypothesis for photoperiodic time measurement in the spider mite.

The photoperiodic clock in blackheaded buntings (Emberiza melanocephala) is mediated by a self-sustaining circadian system

Three experimental protocols were employed to clarify whether the circadian system is involved in photoperiodic time-measurement in the blackheaded bunting, Emberiza melanocephala. In a single-pulse paradigm, one 8-h light pulse was delivered at different times to groups of birds across three days of constant darkness (DD). Photoperiodic induction, as measured by a rise in plasma luteinizing hormone (LH), showed clear circadian rhythmicity. The second experiment examined the LH responses in birds exposed to lighting cycles using a Nanda-Hamner type of protocol and confirmed full photostimulation under 6L:30D. The third experiment measured the time of the first photoinduced rise in LH in birds subjected to 30 h of continuous light following entrainment under short days (6L:18D). This experiment aimed to identify the position of the photoinducible phase (phi i). LH first rose at hour 18 following dawn indicating that phi i lies in the middle of the day. Plasma concentrations of melatonin were also measured under 6L:18D and 6L:30D light cycles as another physiological marker of the circadian systems in buntings. The pattern of melatonin secretion with the driving oscillator being circadian in nature. It is concluded that the circadian pacemaker driving the photoinducible rhythm in blackheaded bunting is strongly self-sustaining and free-runs under constant conditions.

Essential of the environmental control of insect seasonality as reference points for comparative studies in other invertebrates

A great body of knowledge of photoperiodic and other developmental reactions, governing seasonality in insects, may be helpful for similar investigations which are or will be conducted with other animal groups. The following principles, based on a recent hypothesis, seem the most significant to be tested in comparative studies. (1) On the level of the photoperiodic clock only quantitative perception of photoperiod takes place. (2) The following, presumably neuroendocrine, ‘managing’ level of the mechanism discriminates between long and short days, determines the type of the response, and integrates photoperiodic and temperature reactions. (3) A working hypothesis, to be tested with both insects and other invertebrates, is that the ‘managing’ mechanism described in the model of photoperiodic and temperature control of development may have several sensory inputs and, therefore, plays a central role in governing developmental reactions to different environmental cues.

Threshold and quantitative photoperiodic responses exist in an insect

The photoperiodic response for the induction of adult diapause and that for the determination of nymphal body coloration were compared inPlautia stali Scott (Heteroptera: Pentatomidae). The former was an all-or-none response with a distinct threshold, but the latter was a graded response which varied quantitatively with the photophase duration. The photoperiodic clock in this species is discussed.

A pacemaker-slave model for the photoperiodic clock in the vetch aphid, Megoura viciae

Recent investigations into the photoperiodic clock of Megoura viciae indicated that night-length measurement in this aphid is accomplished by a circadian-based oscillator mechanism, despite its typical “hourglass” responses in Nanda-Hamner and Bünsow experiments. To reconcile these apparently contradicting observations, it is suggested here that although long-night determination is executed in a repetitive manner, this is not true for short-night determination. To test this hypothesis, the previously developed “coupled oscillator model” has been modified such that once a scotophase has exceeded the critical night length (as in the Nanda-Hamner experiments) it will always be determined as “long”, no matter whether a subsequent “photo-inducible phase” coincides with darkness or with light. In this respect the modified model differs from all known circadian-clock models. Model-generated responses are compared with a variety of experimental results previously observed with Megoura and the validity of the model as a description of the photoperiodic clock-counter mechanism in Megoura is discussed.

Some effects of low temperature on the photoperiodic clock in Drosophila triauraria

Abstract. Prior studies revealed that the photoperiodic clock in Drosophila triauraria operates during the scotophase and the processes measuring scotophase are composed of two phases: the A phase which lasts 6–7 h from the onset of the scotophase and the B phase which follows the A phase. In this study the photoperiodic clock in this species was analysed by low‐temperature pulses. Low temperature (5d̀C) or a low‐temperature (2d̀C) pulse of 3 or 4 h decreased the induction of diapause when applied during the scotophase, but not when applied within the photophase. The low‐temperature pulse showed two maxima of the effect, 0–4 h and 8–10 h after the onset of the scotophase, approximately corresponding to the A and B phases, respectively. It is considered that low temperature retards the time measurement processes operating during these phases. In the period which was rather insensitive to the diapause‐preventing action of low temperature, i.e. 5‐7h after the onset of the scotophase, substances or stimuli accumulated during the A phase may be converted to information required for operation of the machinery in the B phase. Experiments using a combination of low‐temperature and light pulses suggested that low‐temperature decreases the sensitivity to light, especially in the B phase.

Evidence for ‘dawn’ and ‘dusk’ hourglasses in Pimpla photoperiodic clock

Abstract Resonance experiments (Nanda‐Hamner protocol) conducted at two temperatures for diapause termination in Pimpla instigator (Hymenoptera: Ichneumonidae) do not support the view that the photoperiodic clock has an oscillatory component, but suggest the presence of a non‐rhythmic timer or hourglass mechanism. These results are best explained by a two hourglasses model, one of which starts at light‐on and measures the photophase and the other is initiated by light‐off and measures the scotophase. The most likely hypothesis is that the ratio of photophase to scotophase lengths is the determining element. Good agreement is obtained between results predicted by two hourglasses model and results observed in Pimpla. The diurnal hourglass continues to run for long time (several months) in constant condition (LL) and does not require to be ‘turned over’ by D/L transition, in contrary to the classical model of hourglass which executes a single act of time measurement in extented phase and then stops. The most...

The "Circadian Paradigm": A Test of Involvement of the Circadian System in the Photoperiodic Clock

A long-standing and yet open question is whether the circadian system is involved in photoperiodism. A limited set of protocols were credited with the ability of answering this question. The most widely used are the so-called "resonance experiments". Recent models, however, showed how the working of a non-circadian photoperiodic clock (hourglass) could go with a positive result in resonance experiments, thus giving a strong indication of the unreliability of this test. This paper showed how inferring a series of logical consequences from two properties of circadian system made it possible to describe the behaviour of an ideal circadian photoperiodic clock when submitted to regimes derived from a resonance protocol. This design was dubbed "Circadian paradigm" (CP). Comparing the predicted circadian behaviour with that of a concrete photoperiodic system provided a test of circadian involvement. Application of the CP to an insect species, Pieris brassicae, which gave a positive response to classical resonance experiments, yielded evidence that the inset clock was an hourglass and that the observed circadian modulation could readily be attributed to an inhibitory action of the circadian system on the output of the clock, as proposed by recent models. Another issue was that short- and long-night responses were likely to result from different mechanisms. The CP thus appeared as a theoretical tool fitted to decide whether the circadian system is part of a photoperiodic clock working. The results, which reinforced the grounds for discarding resonance as a circadian test, besides supported some of the theoretical properties of recent models.

The same photoperiodic clock may control induction and maintenance of diapause in the spider mite Tetranchus urticae.

In the spider mite Tetranychus urticae, both diapause induction (which takes place during the larval and nymphal stages) and diapause maintenance (in the adult female) are under photoperiodic control. The question of whether or not the same photoperiodic clock is involved in both photoperiodic reactions was investigated in eight strains of the spider mite, originating from different localities in Europe. The methods employed consisted of (1) determination of the relative importance of the photophase and scotophase in the two photoperiodic reactions; (2) comparison of photoperiodic response curves for diapause induction and diapause maintenance; and (3) determination of the effect of light breaks on the capacity of long nights to maintain diapause, and comparison with the effect of light breaks in diapause induction experiments. The scotophase appeared to be much more important than the photophase for both diapause induction and diapause maintenance. In all strains the critical daylength for diapause maintenance, measured at the moment of saturation of the response to long daylengths, was identical to the critical daylength for diapause induction. However, the critical daylength for diapause maintenance appeared to be labile; it shifted gradually to shorter values as the mites were kept in the cold for a longer period of time, or were kept at a higher temperature for a progressively longer period of time after their stay in the cold room. This seems to reflect a gradual loss of photoperiodic control of diapause maintenance as diapause development proceeds. Photoperiods close to the critical daylength appeared to be less strong with regard to diapause maintenance than shorter daylengths. Quantitative differences in the "strength" of different daylengths were found in all strains investigated. Interruption of the night by short pulses of light revealed either one or two peaks of sensitivity in the night, or one broad "trough" where the two peaks had merged. However, in each case maximal sensitivity to the light breaks occurred at the same position in the night for diapause induction and diapause maintenance. The many similarities found lead to the conclusion that most probably the same photoperiodic clock mechanism is involved in both diapause induction and diapause maintenance in T. urticae.

Circadian rhythmicity is involved in photoperiodic time measurement in the aphidMegoura viciae

The photoperiodic clock in the vetch aphidMegoura viciae is generally accepted to be based on a non-circadian mechanism or “hourglass”, as no evidence has been found for the involvement of the circadian system in the photoperiodic response. By using a recently-devised protocol which discriminates between single and repeated night length measurement, we demonstrate here that long-night measurement inMegoura is executed in a repetitive way, and thus that its photoperiodic clock is based on a circadian oscillator after all. However, it is also apparent that the determination of short nights is not repetitive.

The photoperiodic clock of Drosophila triauraria: Involvement of a circadian oscillatory system

The involvement of the circadian oscillatory system in the photoperiodic induction of reproductive diapause of Drosophila triauraria was examined by the resonance, Bünsow and bistability experiments. When reared with a Nanda-Hamner (resonance) protocol from the egg stage to the 16-day adult stage, this species showed a circadian oscillation in diapause incidence, but the oscillation was gradually damped when the scotophase was extended. When transferred from continuous light to the Nanda-Hamner protocol on the day of eclosion, the insect showed less distinct oscillation. Temperature affected the rate of diapause incidence, but did not affect the pattern of oscillation. On the other hand, the Bünsow and bistability experiments failed to reveal the involvement of the circadian oscillatory system in this photoperiodic clock. These results suggest that the circadian oscillatory system constitutes a part of the photoperiodic clock of this species but plays a limited role in its photoperiodic time measurement. We propose a novel model for the photoperiodic time measurement system of this species.

The photoperiodic clock of Drosophila triauraria: Involvement of two processes in the night-length measurement system

The photoperiodic control of reproductive diapause was examined in Drosophila triauraria. Experiments using non-24 h light-dark cycles revealed that the duration of scotophase plays an essential role for the determination of diapause, and night interruption experiments suggested that the process measuring scotophase was divided into two phases, A and B. The A phase lasted 6 or 7 h from the onset of scotophase, and the light pulse in this phase is assumed to reset the clock. The B phase followed the A phase, and the light pulse in the B phase is assumed sometimes to stop the clock and sometimes to have no effect (i.e. the light pulse seems to be sometimes disregarded). In the A phase, a short light pulse seems to be somewhat less effective to reset the clock than a long one. In the B phase, a short light pulse was disregarded more often than a long one. The relation between these two phases is not known, but substances or stimuli which operate the machinery of the B phase may be accumulated in the A phase, and substances or stimuli responsible for the induction of diapause may be accumulated during the B phase.

Photoperiodic and Thermoperiodic Control of Diapause in Plant-Inhabiting Mites: a Review

The spider mite Tetranychus urticae and the phytoseiid predatory mite Amblyseius andersoni both exhibit a facultative reproductive diapause, which is expressed in females only. Profound similarities of a qualitative nature were found in responses to photoperiod of these two species, which might indicate the presence of a common physiological basis for the photoperiodic induction of diapause. These similarities concern the use of vitamin A (or a derivative of vitamin A) as photoreceptor pigment for the photoperiodic clock, and the nature of the photoperiodic clock and photoperiodic 'counter', i.e. the mechanism that accumulates and integrates the output of the photoperiodic clock over a sequence of light/dark cycles. The spider mite and predatory mite differ in their response to temperature. Whereas daily fluctuating temperatures (thermoperiods) induce diapause in A. andersoni in the complete absence of light, no such thermoperiodic response could be detected in T. urticae. Some striking similarities were demonstrated between the photoperiodic and thermoperiodic response mechanisms in the predatory mite. The results strongly suggest that photoperiodic and thermoperiodic induction of diapause in A. andersoni are based on the same physiological mechanism. Similarities between the photoperiodic response mechanisms of mites and insects are discussed. The common interpretation of the role of the circadian system in the photoperiodic response mechanism of insects and mites is criticized and an alternative explanation of circadian effects on photoperiodic phenomena is presented.

Photoperiodic induction of winged females in the black bean aphid. Aphis fabae

Abstract. The Photoperiodic of winged females (alatae) in the black bean aphid, Aphis fabae Scop. (Homopetera: Aphididae), is investigated in detail with emphasis on the interaction of the maternal and embryonic/young larval photoperiodic clocks. Previous work had shown that in uncrowded conditions the induction of gynoparae (winged females that produce sexual females) requires both prenatal and postnatal exposure to long‐night (12 h) Photoperidic cycles: present results show that sole postantal exposure to long nights of any lenght does not induce wing formation in early‐born aphids.When aphids were exposed to experimental light‐dark cycles postanatally only, their daughters developed as alate in long nights and as apterae in short nights: the critical night lenght (CNL) was 11:1 h. Additional prenatal exposure to experimental regimes resulted in a significantly shorter CNL (10.6 h). This difference could be accounted for by the fact that more experimental light‐dark cycles were experienced in the latter case.Apterous aphids transferred from LD 16:8 h to LD 12:12 h as either third‐or fourth‐stadium larvae, or young adults, switched for aptera‐production to alata‐production. The transition form aptera‐ to alata‐production was rather abrupt in third‐stadium transfers but more gradual when transfers occurred as fourth‐stadium larvae and adults. Moreover, s the number of days required for 50% of the aphids to become alata‐producers increased from 7–8 in third‐stadium transfers, to 9–10 and 11–12 in the later transfers.

Circadian nature of the photoperiodic clock in Japanese quail.

The photoperiodic clock in quail (Coturnix coturnix japonica) is based upon a rhythm of photoinducibility (phi i) but the extent to which this rhythm is circadian remains unclear. Two types of experiment investigated this situation. In the first, gonadectomized quail were adapted to live in periods of darkness by training them on a schedule containing one short day and 3 days of darkness (SD/DD/DD/DD). They were then exposed to a single pulse of 6 or 10 h of light at different times across 3 days of darkness. The photoperiodic response, measured by the increase in LH secretion, showed clear rhythmicity, demonstrating unequivocally the circadian nature of phi i. The second set of experiments employed Nanda-Hamner cycles and varied the length of the photoperiod from 6 to 11 h. Responsiveness in a 36 h or a 60 h cycle was highly dependent upon the length of the photoperiod, something not predicted from theory. For instance, LD 6:30 was not photoperiodically inductive but LD 10:26 was clearly inductive. Close analysis of patterns of LH secretion indicated an unexpected delay before induction occurred and then a rapid rise to a stable level of induction. When LH was measured in every pulse under LD 10:26 there was no evidence that LH levels alternately increased and decreased. This is not consistent with the simplest interpretation of Nanda-Hamner experiments where alternate pulses of light are thought to "entrain" the rhythm or "induce" a photoperiodic response by coinciding with phi i. It is concluded that the quail's photoinducible rhythm is indeed based on a circadian rhythm but one that is only weakly self-sustaining.(ABSTRACT TRUNCATED AT 250 WORDS)

A coupled pacemaker-slave model for the insect photoperiodic clock: interpretation of ovarian diapause data in Drosophila melanogaster.

A coupled circadian oscillator model for the insect photoperiodic clock is described which consists of a hierarchically arranged pacemaker and slave. The pacemaker is self-sustained, temperature compensated, and entrainable by the light cycle; the slave is a damping oscillation receiving entrainment from two sources, from the pacemaker via a coupling factor, and also directly from the light. The damping slave oscillation is seen as the "photoperiodic oscillator", equivalent to that proposed earlier by Lewis and Saunders (1987). The present simulations describe the effect of the strength of the coupling factor between hypothetical short- and long-period pacemaker oscillations (modelled on the "clock" mutants perS and perL2 in Drosophila melanogaster) and a slave oscillation with a period of about 24 hours. The output is presented in terms of photoperiodic response curves and Nanda-Hamner, or resonance, plots. With a high coupling strength, the pacemakers strongly entrain the slave, but with a low coupling strength the slave's properties are more evident. The model is presented as a possible explanation for recent ovarian diapause data in D. melanogaster "clock" mutants (Saunders 1990), but also as a more general model for the role of the insect circadian system in seasonal time measurement.